Critical Dynamics in the Association Cortex Predict Higher Intelligence in Typically Developing Children

Neuronal network models have indicated that the so-called critical dynamics facilitate efficient information processing, while criticality disruptions were linked to neuropathology through excitation/inhibition (E/I) imbalances. However, there is limited empirical evidence for a relationship between critical brain dynamics and cognition in healthy children and adolescents. Here, we investigate how these dynamics relate to intelligence in a developing cohort. We recorded eyes-open resting EEG in 128 children (6-19 years, 72 female) and quantified near-critical dynamics in the alpha-band using functional excitation/inhibition ratio (fE/I) and in nonoscillatory activity using the 1/f aperiodic exponent of the power spectrum. We devised models relating intelligence to fE/I and 1/f exponent across seven Yeo7 functional brain networks ranked from lower-order sensorimotor to higher-order association networks. We observed significant correlations between fE/I and 1/f exponent and IQ in association cortices, in contrast to sensorimotor cortices. Children in the high-IQ group had fE/I ratios closer to the theoretical critical value of 1 in association cortices compared with the low-IQ group. The association-sensorimotor axis rank moderated the associations between 1/f exponent and IQ, these associations decreasing on a gradient across the hierarchy of the Yeo7 networks. Age and rank moderated the fE/I-IQ association, with the association-sensorimotor effect size gradient most visible in adolescents. Together, the results suggest that individual variation in criticality-sensitive biomarkers in association networks may be linked to IQ differences in an age-dependent manner, consistent with the hypothesis that developmental modulation of critical dynamics across the cortical hierarchy may support more efficient cognitive processing.